Structure of the bacteriophage φ29 DNA packaging motor

Alan A. Simpson; Yizhi Tao; Petr G. Leiman; Mohammed O. Badasso; Yongning He; Paul J. Jardine; Norman H. Olson; Marc C. Morais; Shelley Grimes; Dwight L. Anderson; Timothy S. Baker; Michael G. Rossmann

doi:10.1038/35047129

Structure of the bacteriophage φ29 DNA packaging motor

Alan A. Simpson, Yizhi Tao, Petr G. Leiman, Mohammed O. Badasso, Yongning He, Paul J. Jardine, Norman H. Olson, Marc C. Morais, Shelley Grimes, Dwight L. Anderson, Timothy S. Baker, Michael G. Rossmann

Diagnostic and Biological Sciences

Research output: Contribution to journal › Article › peer-review

458 Scopus citations

Abstract

Motors generating mechanical force, powered by the hydrolysis of ATP, translocate double-stranded DNA into preformed capsids (proheads) of bacterial viruses and certain animal viruses. Here we describe the motor that packages the double-stranded DNA of the Bacillus subtilis bacteriophage φ29 into a precursor capsid. We determined the structure of the head-tail connector-the central component of the φ29 DNA packaging motor-to 3.2Å resolution by means of X-ray crystallography. We then fitted the connector into the electron densities of the prohead and of the partially packaged prohead as determined using cryo-electron microscopy and image reconstruction analysis. Our results suggest that the prohead plus dodecameric connector, prohead RNA, viral ATPase and DNA comprise a rotary motor with the head-prohead RNA-ATPase complex acting as a stator, the DNA acting as a spindle, and the connector as a ball-race. The helical nature of the DNA converts the rotary action of the connector into translation of the DNA.

Original language	English (US)
Pages (from-to)	745-750
Number of pages	6
Journal	Nature
Volume	408
Issue number	6813
DOIs	https://doi.org/10.1038/35047129
State	Published - Dec 7 2000

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title = "Structure of the bacteriophage φ29 DNA packaging motor",

abstract = "Motors generating mechanical force, powered by the hydrolysis of ATP, translocate double-stranded DNA into preformed capsids (proheads) of bacterial viruses and certain animal viruses. Here we describe the motor that packages the double-stranded DNA of the Bacillus subtilis bacteriophage φ29 into a precursor capsid. We determined the structure of the head-tail connector-the central component of the φ29 DNA packaging motor-to 3.2{\AA} resolution by means of X-ray crystallography. We then fitted the connector into the electron densities of the prohead and of the partially packaged prohead as determined using cryo-electron microscopy and image reconstruction analysis. Our results suggest that the prohead plus dodecameric connector, prohead RNA, viral ATPase and DNA comprise a rotary motor with the head-prohead RNA-ATPase complex acting as a stator, the DNA acting as a spindle, and the connector as a ball-race. The helical nature of the DNA converts the rotary action of the connector into translation of the DNA.",

author = "Simpson, {Alan A.} and Yizhi Tao and Leiman, {Petr G.} and Badasso, {Mohammed O.} and Yongning He and Jardine, {Paul J.} and Olson, {Norman H.} and Morais, {Marc C.} and Shelley Grimes and Anderson, {Dwight L.} and Baker, {Timothy S.} and Rossmann, {Michael G.}",

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doi = "10.1038/35047129",

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AU - Simpson, Alan A.

AU - Tao, Yizhi

AU - Leiman, Petr G.

AU - Badasso, Mohammed O.

AU - He, Yongning

AU - Jardine, Paul J.

AU - Olson, Norman H.

AU - Morais, Marc C.

AU - Grimes, Shelley

AU - Anderson, Dwight L.

AU - Baker, Timothy S.

AU - Rossmann, Michael G.

PY - 2000/12/7

Y1 - 2000/12/7

N2 - Motors generating mechanical force, powered by the hydrolysis of ATP, translocate double-stranded DNA into preformed capsids (proheads) of bacterial viruses and certain animal viruses. Here we describe the motor that packages the double-stranded DNA of the Bacillus subtilis bacteriophage φ29 into a precursor capsid. We determined the structure of the head-tail connector-the central component of the φ29 DNA packaging motor-to 3.2Å resolution by means of X-ray crystallography. We then fitted the connector into the electron densities of the prohead and of the partially packaged prohead as determined using cryo-electron microscopy and image reconstruction analysis. Our results suggest that the prohead plus dodecameric connector, prohead RNA, viral ATPase and DNA comprise a rotary motor with the head-prohead RNA-ATPase complex acting as a stator, the DNA acting as a spindle, and the connector as a ball-race. The helical nature of the DNA converts the rotary action of the connector into translation of the DNA.

AB - Motors generating mechanical force, powered by the hydrolysis of ATP, translocate double-stranded DNA into preformed capsids (proheads) of bacterial viruses and certain animal viruses. Here we describe the motor that packages the double-stranded DNA of the Bacillus subtilis bacteriophage φ29 into a precursor capsid. We determined the structure of the head-tail connector-the central component of the φ29 DNA packaging motor-to 3.2Å resolution by means of X-ray crystallography. We then fitted the connector into the electron densities of the prohead and of the partially packaged prohead as determined using cryo-electron microscopy and image reconstruction analysis. Our results suggest that the prohead plus dodecameric connector, prohead RNA, viral ATPase and DNA comprise a rotary motor with the head-prohead RNA-ATPase complex acting as a stator, the DNA acting as a spindle, and the connector as a ball-race. The helical nature of the DNA converts the rotary action of the connector into translation of the DNA.

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Structure of the bacteriophage φ29 DNA packaging motor

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